Metamorphosis

Metamorphosis, a term used in zoology in different senses by different authors, and sometimes in different senses by the same author. E. Korschelt and K. Heider, in their work on the development of the Invertebrata, usually apply it to the whole of the larval development. For instance, in their account of the Bryozoa, they say (p. 18, part 2, of the English translation): "The metamorphosis of a Bryozoan larva comprises a more or less protracted free-swimming stage during which no perceptible advance is made in the development of the larva, and the subsequent somewhat complicated changes which bring about its transformation into the first primary zooid of the young Bryozoan colony." Throughout their account of the Crustacea they use the word in the same sense, i.e. as applied to the whole of the changes which the larva undergoes in passing into the adult. On the other hand, in their account of Mollusca they seem to restrict the term to the final change by which the larva passes into the adult form (op. cit., part 4, p. 14). F. Balfour in his great work on Comparative Embryology seems to limit the word to a sudden change in the larval history. For instance, he says: "The chief point of interest in the above development is the fact of the primitive nauplius form becoming gradually converted without any special metamorphosis into the adult condition" (Comparative Embryology, 1885, i. 463). "By the free Cypris stage into which the larva next passes a very complete metamorphosis has been effected" (op. cit. i. 490). "The change undergone by the Tadpole in its passage into the Frog is so considerable as to deserve the name of a metamorphosis" (op. cit. ii. 137). Finally and most decisively he says in his general account of larvae: "In the larval type [of development] they are born at an earlier stage of development, in a condition differing to a greater or less extent from the adult, and reach the adult state either by a series of small steps or by a more or less considerable metamorphosis" (op. cit. ii. 360). Here the term will be used in the sense of the last quotations from Balfour and will be regarded as applicable only to those cases of sudden and marked change which frequently occur at the end of the larval period and sometimes at more or less frequent intervals during its course (Crustacea).

Some authors (see H. G. Bronn, Thierreich, " Myriapoda," Bd. 5, Abth. 2, p. 113) have applied the term "metamorphosis" only to those cases of larval development in which the young leaves the egg with provisional organs which are lost in the later development. Such authors apply the term "anamorphosis" to cases in which the just-hatched young is without provisional organs but differs from the adult in size, and in the number of segments and joints, &c. Such writers apply the term "epimorphosis" when there is merely an acquisition of sexual maturity and increase in size after birth or hatching.

The essential feature of metamorphosis is the sudden bursting into function of new organs, whether these organs suddenly arise or have been gradually formed, without becoming functional in preceding larval stages. Another feature of it is the disappearance of organs which have been of use to the larva but which are not required at all or are not required in the same form in the new environment. The term is only used in connexion with larval development and is not applied to the sudden changes, due to a change of environment (e.g. the passage of the mammalian embryo from the oviduct into the uterus), which sometimes occur in embryos. Neither is it used in connexion with the sudden changes of conditions which occur at the birth or hatching of an embryo, although, especially in the case of birth, this event is frequently accompanied by profound morphological alteration.

The most familiar examples of metamorphosis are the abrupt changes which occur at the end of the larval history of the frog and of many insects. In both these cases there is a sudden and great change of environment; there is a sudden demand for new organs which would have been quite useless in the old environment, and organs which were of use in the old environment and are of no use in the new have to be eliminated. The two examples we have chosen have the advantage of showing us the two methods by which the crisis in the life-history is met.

In the frog (fig. I) the structural changes which obtain full fruition at the metamorphosis take place gradually during the previous tadpole life. They relate mainly to the alterations of the respiratory organs and vascular system which are required for the purely terrestrial life of the frog, and to the appearance of the paired limbs. The changes in the respiratory and vascular After Leuckart and Nitsche's Wandtafeln, by permission of T G. Fisher & Co.

FIG. 1. - Drawings illustrating the metamorphosis of the frog (Rana temporaria).  A, Side view of an advanced tadpole with well-developed posterior limbs; the anterior limbs are present but hidden beneath the operculum.

B, Ventral view of the same with operculum removed showing the anterior limbs in situ; the ventral body wall has also been removed and the heart (ht) and intestine exposed. (br) Gills; (KL) spiracle.

C, A frog after the metamorphosis but before the absorption of the tail.

organs are led up to in the tadpole, which during the greater part of its aquatic life is a truly amphibious animal, breathing by lungs as well as by gills; but a sudden change occurs in these organs at the metamorphosis. The limbs which were slowly formed during tadpole life - the posterior pair visibly, the anterior under cover of the operculum (fig. 1, B) - are of no use to the tadpole and must constitute a pure burden to it. The principal events of the metamorphosis are the sudden appearance of the anterior limbs, and the complete closure of the gill aperture (fig. 1, C). The appearance of the anterior limbs and the acquisition of functional importance by both pairs enable the frog to leave the water and pass on to the land to lead its terrestrial life. The other larval organs, such as the gills and the tail, gradually shrink in size and ultimately vanish. In the case of the gills this shrinkage had begun before the meta morphosis, but the tail shows no sign of diminution until the frog is ready to pass on to the land.

The distinguishing feature of this type of metamorphosis is that the animal is burdened for a certain period, both before and after, with organs which are useless to it. In the next type, which is exemplified by the metabolous Insecta, this occurs to a much smaller extent, although the changes of habitat and the corresponding changes of structure are more remarkable. In insecta the change is usually from a terrestrial or aquatic habitat to an aerial one. The larva of a butterfly is a worm-like organism which creeps on and voraciously devours the foliage of certain plants (fig. 2, C). During its life it undergoes much growth, but no important change in structure. When it leaves the egg it is adapted to live and feed on a particular species of plant, on or near which the eggs are deposited by the parent butterfly. It has powerful biting jaws by which it procures its vegetable food. The adult, on the other hand, is a winged creature which also lives on plants but in quite a different way to the larva (fig. 2, A). It flies from plant to plant and obtains its food by sucking the juices of flowers and other parts. The powerful mandibles of the larva have disappeared and in their place we find a suctorial proboscis s formed by the first maxillae [fig. 2, A (4)].

  


Between the larva and the adult insect there is interposed a resting stage, the so-called pupa (fig. 2, B), during which no food is taken, but very important changes of structure occur. These changes consist of two processes: (I) histolysis, by which most of the larval organs are destroyed by the action of phagocytes; and (2) histogenesis, by which the corresponding organs of the imago are developed from the imaginal disks. The imaginal disks ap pear to arise in the embryo in which they develop, some of them from the epiblast and some from the hypoblast. They persist practically unchanged through larval life and become active as centres of growth in the pupa. The pupal stage in such a metamorphosis may be compared to a second embryonic stage in which the organs of the adult assume their final shape. In this kind of metamorphosis the larval organs are entirely got rid of in the pupal stage, during which the insect is as a rule incapable of locomotion and takes no food; and the new formation of organs - especially those of locomotion and alimentation - which is necessitated by the totally different habits of the larva and mature insect, is also accomplished at the same period, largely, no doubt, at the expense of the material afforded by the disrupted larval organs. The larva itself does not form any of these organs and carry them about during its active life, though it does possess the very minute centres of growth known as the imaginal disks which burst into activity after the larval life is over. It must not be supposed that in all insects in which the sexual animal has a different habitat from the young form, there is a metamorphosis of the kind just described. In the may-flies and dragon-flies, in which the larva is aquatic, the change is prepared for some time before the actual metamorphosis, the organs which are necessary for the aerial existence being gradually acquired during larval life. In such cases, the metamorphosis belongs to our first type and consists of the act by which the organs previously and gradually acquired suddenly become functional. We have now considered in detail two typical cases of metamorphosis. In the first the change is gradually led up to and the larva is burdened, in its later stages at least, with organs which are of no use to it and only become functional at the metamorphosis. In the other, the change is not led up to. It is sudden, and a kind of second embryonic period is established After Leuckart and Nitsche's Wandtafeln, by permission of T. G. Fisher & Co.

FIG. 2. - Three stages in the lifehistory of the cabbage butterfly, Pieris brassicae, L.

A, Imago (female), side view.

B, Pupa fixed by a cord across the middle of the body and by the tail.

C, Caterpillar.

(I) Forewing; (5) thoracic legs; (2) antenna; (6) hind wing; (3) labial palp; (7) the head; (4) first maxilla; (8) the thorax; (q) the abdomen, some of the segments of which in the caterpillar carry a pair of prolegs (to).

to enable the important and far-reaching transformation to be accomplished. It is clear that the two kinds of metamorphosis a3 at 82 E A and B after Fritz Muller in Archiv. fiir Naturgeschichte, vol. xxix., 186 3; C, D, and E after C. Claus, Untersuch. zur Erforschung Crustaceen-Systems.  FIG. 3. - Drawings showing various stages in the larval history of Penaeus.  A, Nauplius larva, dorsal view, showing the three pairs of appendages and the simple median eye.

B, Protozoaea larva, dorsal view, the rudiments of the paired eyes are visible through the cuticle, by which the rudiments of the maxillae are still covered.

C, Older Protozoaea, dorsal view; the six posterior thoracic segments are distinct, but the five abdominal segments are still hidden beneath the skin.

D, Zoaea larva, ventral view, with the rudiments of the thoracic limbs and the appendages of the sixth abdominal segment.

E, Mysis stage, side view; the thoracic and abdominal appendages have been developed.

(I) first antenna; (9) thorax; (2) second „ (I o) abdomen; (3) mandible; (I I) liver; (4) first maxilla; (12) frontal sense organ, just be (5) second „ hind which are the compound (6) first maxilliped; eyes; (7) second „ (ai) to (a6) the six abdominal (8) third „ appendages.

only differ in degree and that no line can be drawn between them.

In the Crustacea, as has already been pointed out, many authors apply the term metamorphosis to the whole larval development, which consists of a series of changes leading to the adult form. But this is in our opinion an incorrect use of the word. The typical larval development of a Crustacean consists of a series of small metamorphoses. At each moult new organs which have been developed since the preceding moult become manifest and some of them functional. For instance, the prawn Penaeus leaves the egg as a nauplius larva (fig. 3, A). It issues from the first moult as a metanauplius which has a forked tail, a beginning of the cephalo-thoracic shield, and a large helmet-shaped upper lip. It also possesses stump-like rudiments of the maxillae and two anterior pairs of maxillipeds. After the next moult it is known as a protozoaea (fig. 3, B), in which a cephalo-thoracic shield is well developed, the posterior part of the body is prolonged into a tail, in the anterior part of which the thoracic segments are obscurely indicated, and the four pairs of stump-like rudiments have become functional appendages [fig. 3, B (4), (5), (6), (7)]. This passes into a later protozoaea stage (C) in which the rudiments of the compound eyes and of the abdominal segments are visible beneath the cuticle and in which certain functional changes (jointing, &c.) have appeared in the limbs. This is succeeded by the zoaea stage (fig. 3, D), characterized by the stalked and functional condition of the eyes, the increased size of the abdominal segments, and the appearance of appendages on the sixth of them, the increase of size in the third pair of maxillipeds (8) which had appeared as small rudiments in the preceding stage, and the appearance of the five pairs of posterior thoracic limbs as small biramous appendages. The zoaea stage is followed by the mysis stage (fig. 3, E) in which the thoracic feet are biramous, as in Mysis. From this the adult form proceeds. The transformation is more gradual than would be gathered from this short description, because moults After C. Claus, Untersuch. zur Erforschung Crustaceen-Systems.  FIG. 5. - Metanauplius larva of Balanus (Naples), immediately preceding the Cypris larva; ventral view. The six pairs of biramous appendages of the Cypris stage are visible beneath the cuticle. The median simple eye and the compound eye are both visible.

(I) first antenna; (2) second „ (3) mandibles; (4) rudiment of the maxilla; (5) first pair of biramous limbs; (6) sixth „ (7) upper lip; (8) frontal sense organs.

occur during the later stages from each of which the larva comes with some slight transformation.

In the life-history of a typical Cirripede there may be said to be two distinct metamorphoses, with gradual developmental stages taking place between them. The animal is hatched as a nauplius. This undergoes a series of moults during which increase in size and slight changes in form occur (fig. 4, A, B). At the last of them several organs characteristic of the second After Spence Bate in Annals and Magazine of Nat. History, vol. 8, and series, 1851.

FIG. 4. - Nauplius of Balanus balanoides.  A, As just hatched; B, After the first moult.

(I) first pair of nauplius appendages; (2) second „ (3) third „ (4) upper lip; (5) frontal sense organ.

or Cypris stage are discernible [fig. 5 (5), (6)1 beneath the cuticle. When this is moulted the free-swimming cypris larva is liberated with its six pairs of biramous thoracic legs, its bivalve shell, and its paired compound eyes (fig. 6). This is the first metamorphosis. After a certain period of free life the Cypris larva attaches itself by its anterior antennae to some foreign object and enters upon the pupal stage (fig. 7). During this the larva takes no food and ceases to move, and undergoes important changes of structure and form beneath the larval cuticle, which invests it like a pupal case. These changes lead to the 8 After C. Claus, Schriften der Gesellsch. zur Beford. der gesammten Naturwissen.  zu Marburg.  FIG. 6. - Cypris larva fascicularis.  (I) first antenna; (2) compound eye; (3) simple eye; (4) biramous appendages.

attainment of the adult form and structure. When they are completed the cuticle, including the shell-valves, is cast off and the young cirriped emerges. This is the second and final metamorphosis, which resembles in its main features the metamorphosis of the metabolous Insecta.

Metamorphosis occurs in most groups of the animal kingdom. It is generally found in attached organisms, for these nearly always have free-swimming larvae and the metamorphosis occurs when the change of habit is effected. For the details of the process the reader is referred to systematic works on zoology. Here only the most striking instances of it can be mentioned. It occurs in a remarkable form in some sponges, in which at the metamorphosis the larval epidermis, which acts as a locomotive organ, is said to become transformed into the collared flagellated cells of the canal system, the adult epidermis being a new formation. It occurs in the Polyzoa, and is, in some of these, characterized by an almost complete disruption of the larval organs and a subsequent new formation of the organs of the adult. The metamorphosis in such cases belongs to our second type, the new organs being new formations at the metamorphosis and not developed from rudiments which make their appearance in the earlier larval history. In Phoronis the metamorphosis of the larva (Actinotrocha), which occurs on fixation, is gradually led up to, but the mode of destruction of some of the larval organs is peculiar; the brain and sense organs of the larva pass into the stomach and are digested. In the Tunicata, in which fixation of the free larva is effected by the head, as in Cirripedia and some, if not all, Polyzoa, the metamorphosis occurs entirely after fixation as a rapid series of developmental changes which occur ad hoc and are not prepared for by preceding changes. In Amphioxus there is no metamorphosis though the larval changes are most remarkable and extensive, but the larval life is a long one and the development very gradual, the new organs coming into function as soon as they are formed.

In most Mollusca there is also a prolonged and important larval life, marked by very interesting stages of structure (trochosphere, veliger, &c.), but it is not usual to speak of a metamorphosis for the changes are gradual, each organ developing with great rapidity and coming into function at once. In certain forms, however, a metamorphosis occurs, e.g.  in the glochidium larva of Anodonta, which embeds itself in the skin of a fish and there metamorphoses into the adult.

In the Echinodermata there is a particular stage in the larval history, when the ciliary locomotive apparatus breaks up and is absorbed and the animal takes to its creeping adult life. This metamorphosis is gradually prepared for in the precedent larval development by changes which ultimately lead to the complete establishment of the adult radial symmetry. The metamorphosis belongs therefore to our first type, but it is remarkable for the heavy burden of adult structures which the larva, in its later stages at least, carries about (fig. 8). The adult body is, in the main, fashioned out of the larval body, and it takes over most of the organs of the latter; but as a rule the adult mouth, oesophagus and anus are new formations, and the central nervous system of the larva when present shares the fate of the larval locomotory apparatus. In Asteroids and Crinoids the metamorphosis is accompanied by fixation to foreign objects, the fixation being effected as in Cirripedes by the preoral lobe.

In the Vertebrata a metamorphosis occurs in the lamprey and the Amphibia. The metamorphosis of the lamprey is peculiar. It lives for three or four years as a sexless larva, known as the ammocoete. It then quite rapidly (in three or four days) undergoes a series of changes and becomes converted into the adult. The metamorphosis affects the alimentary canal, the eyes, the respiratory apparatus and other organs, and especially the reproductive organs, which become mature. The adult lives for a few months only, spawning soon after the metamorphosis. This metamorphosis belongs to our second type, but there does not appear to be any resting stage during the few days in which it is effected. In the Amphibia the metamorphosis is fairly exemplified by that of the frog. In many fishes there is a considerable larval development, but this is perfectly gradual and there does not appear to be anything of the nature of a metamorphosis.

In most cases of metamorphosis those organs of the larva, which are found also in the adult, persist through the transformation, undergoing merely the ordinary modifications of development. But it sometimes happens that such organs are completely destroyed and rebuilt during the metamorphosis. This is conspicuously the case in the metabolous Insecta, in some of which all the internal organs undergo disruption and are reformed. It happens also in those nemertine worms which develop by a larva; in these the larval epidermis is cast off, a new one having been formed. It is possible that the same phenomenon occurs in sponges. In most Echinoderms a similar phenomenon is observed with regard to the oesophagus and the mouth and anus. The probable explanation of this remarkable phenomenon would appear to be that in certain cases the larval organs become so highly specialized in connexion with the larval life that they are unable to undergo further change; new formation is therefore necessary. The phenomenon is one of considerable interest, for it is found in the case of the blastopore, in cases in which there is no metamorphosis, sometimes even in embryonic development. There can be little doubt that the mouth and anus are both genetically connected with the earlier blastopore and that the blastopore is homologous in most animals; and yet how seldom does the blastopore become transformed into the adult openings and how various is its fate. The hypothesis suggested above applies completely to this behaviour of the blastopore; that is to say, it is suggested that the primitive mouth or blastopore becomes, or has become in some vanished larval history, so highly specialized in connexion with larval needs that it is unable to give rise to both mouth and anus, and in some cases to either. (A. SE.*)